Neonatal isolation decreases cued fear conditioning and frontal cortical histone 3 lysine 9 methylation in adult female rats

Kao, Gour Shenq; Cheng, Ling; Chen, Li Hsien; Tzeng, Wen Yu; Cherng, Chienfang G.; Su, Chien-Chou; Wang, Ching Yi; Yu, Lung

doi:10.1016/j.ejphar.2012.09.040

Cited by 28 publications

(20 citation statements)

References 33 publications

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“…Attenuated basal corticosterone concentrations have been observed in adult rats exposed to early life stress in the forms of maternal separation/neonatal handling (Faure et al, 2006; Haley et al, 2013; Panagiotaropoulos et al, 2004; Papaioannou et al, 2002; Slotten et al, 2006), postnatal novelty exposure (Tang et al, 2003), and restraint given to pregnant dams (Belay et al, 2011). However, others have observed either no difference or increased basal corticosterone concentrations following early life stress (Kao et al, 2012; Lukkes et al, 2009; Tiba et al, 2008; Veenema and Neumann, 2009). Interestingly, juvenile offspring of dams given corticosterone in the drinking water also display decreased basal corticosterone concentrations (McCormick et al, 2001), similar to the effect observed in the juvenile offspring in the present study.…”

Section: Discussionmentioning

confidence: 96%

Transgenerational effects of social stress on social behavior, corticosterone, oxytocin, and prolactin in rats

Babb

Carini

Spears

et al. 2014

Hormones and Behavior

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Social stressors such as depressed maternal care and family conflict are robust challenges which can have long-term physiological and behavioral effects on offspring and future generations. The current study investigates the transgenerational effects of an ethologically relevant chronic social stress on the behavior and endocrinology of juvenile and adult rats. Exposure to chronic social stress during lactation impairs maternal care in F0 lactating dams and the maternal care of the F1 offspring of those stressed F0 dams. The overall hypothesis was that the male and female F2 offspring of stressed F1 dams would display decreased social behavior as both juveniles and adults and that these behavioral effects would be accompanied by changes in plasma corticosterone, prolactin, and oxytocin. Both the female and male F2 offspring of dams exposed to chronic social stress displayed decreased social behavior as juveniles and adults, and these behavioral effects were accompanied by decreases in basal concentrations of corticosterone in both sexes, as well as elevated juvenile oxytocin and decreased adult prolactin in the female offspring. The data support the conclusion that social stress has transgenerational effects on the social behavior of the female and male offspring which are mediated by changes in the hypothalamic–pituitary–adrenal axis and hypothalamic–pituitary–gonadal axis. Social stress models are valuable resources in the study of the transgenerational effects of stress on the behavioral endocrinology of disorders such as depression, anxiety, autism, and other disorders involving disrupted social behavior.

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Section: Discussionmentioning

confidence: 96%

Transgenerational effects of social stress on social behavior, corticosterone, oxytocin, and prolactin in rats

Babb

Carini

Spears

et al. 2014

Hormones and Behavior

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“…Interestingly, these epigenetic changes were also observed in the sperm of MS-reared males and may account for the transmission of behavioral and epigenetic effects of MS-rearing across generations (21, 71). Beyond DNA methylation, there is also evidence for post-translational modification to histones associated with MS-rearing and pharmacological inhibition of histone deacetylases prior to MS can prevent the emergence of MS-associated risk phenotypes (72–74). Comparison of B6 and Balb/c mice on MS-induced histone changes suggests that altered cortical histone deacetylase mRNA (increased in juveniles and decreased in adults) is associated with MS-rearing in Balb/c but not B6 mice and that these enzymatic changes are associated with age-dependent differences in histone (H4) acetylation (73).…”

Section: Discussionmentioning

confidence: 99%

Sex-Specific and Strain-Dependent Effects of Early Life Adversity on Behavioral and Epigenetic Outcomes

Kundaković¹,

Lim²,

Gudsnuk³

et al. 2013

Front. Psychiatry

148

145

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Early life adversity can have a significant long-term impact with implications for the emergence of psychopathology. Disruption to mother-infant interactions is a form of early life adversity that may, in particular, have profound programing effects on the developing brain. However, despite converging evidence from human and animal studies, the precise mechanistic pathways underlying adversity-associated neurobehavioral changes have yet to be elucidated. One approach to the study of mechanism is exploration of epigenetic changes associated with early life experience. In the current study, we examined the effects of postnatal maternal separation (MS) in mice and assessed the behavioral, brain gene expression, and epigenetic effects of this manipulation in offspring. Importantly, we included two different mouse strains (C57BL/6J and Balb/cJ) and both male and female offspring to determine strain- and/or sex-associated differential response to MS. We found both strain-specific and sex-dependent effects of MS in early adolescent offspring on measures of open-field exploration, sucrose preference, and social behavior. Analyses of cortical and hippocampal mRNA levels of the glucocorticoid receptor (Nr3c1) and brain-derived neurotrophic factor (Bdnf) genes revealed decreased hippocampal Bdnf expression in maternally separated C57BL/6J females and increased cortical Bdnf expression in maternally separated male and female Balb/cJ offspring. Analyses of Nr3c1and Bdnf (IV and IX) CpG methylation indicated increased hippocampal Nr3c1 methylation in maternally separated C57BL/6J males and increased hippocampal Bdnf IX methylation in male and female maternally separated Balb/c mice. Overall, though effect sizes were modest, these findings suggest a complex interaction between early life adversity, genetic background, and sex in the determination of neurobehavioral and epigenetic outcomes that may account for differential vulnerability to later-life disorder.

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“…Further, aberrant histone methylation has been associated with multiple psychiatric disorders (Akbarian and Huang, 2009, Huang et al, 2007). Less is known regarding histone methylation after early-life stress (Kao et al, 2012), but it is likely that our model elicits changes in histone methylation at bdnf promoters. It will be important in future studies to investigate repressive chromatin marks, such as H3K9 methylation, to see if these are likewise affected.…”

Section: Future Directionsmentioning

confidence: 99%

Long-term effects of early-life caregiving experiences onbrain-derived neurotrophic factorhistone acetylation in the adult rat mPFC

Blaze

Asok

Roth

2015

Stress

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Infant-caregiver experiences are major contributing factors to neural and behavioral development. Research continues to indicate that epigenetic mechanisms provide a way in which infant-caregiver experiences affect gene activity and other downstream processes in the brain that influence behavioral development. Our laboratory previously demonstrated in a rodent model that exposure to maltreatment alters methylation of DNA associated with the brain derived neurotrophic factor (bdnf) and reelin genes as well as mRNA of key epigenetic regulatory genes in the medial prefrontal cortex (mPFC). In the current study we characterized patterns of histone acetylation at bdnf and reelin gene loci after our caregiver manipulations. Using a within-litter design (n=8–10/group from 8 litters), pups were exposed to adverse (maltreatment condition: exposure to a stressed caregiver) or nurturing (cross-foster condition: exposure to a nurturing caregiver) caregiving environments outside the home cage for 30 minutes each day during the first postnatal week. Remaining pups in a litter were left with the biological mother during each session (providing normal care controls). We then used chromatin immunoprecipitation (ChIP) and quantitative RT-PCR to measure histone 3 lysine 9/14 acetylation at bdnf exons I and IV and the reelin promoter in the adult mPFC. Maltreated females had decreased acetylation at bdnf IV, while neither males nor females exhibited histone acetylation alterations at bdnf I or the reelin promoter. These data demonstrate the ability of maltreatment to have long-term consequences on histone acetylation in the mPFC, and provide further evidence of the epigenetic susceptibility of bdnf IV to the quality of infant-caregiver experiences.

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Neonatal isolation decreases cued fear conditioning and frontal cortical histone 3 lysine 9 methylation in adult female rats

Cited by 28 publications

References 33 publications

Transgenerational effects of social stress on social behavior, corticosterone, oxytocin, and prolactin in rats

Transgenerational effects of social stress on social behavior, corticosterone, oxytocin, and prolactin in rats

Sex-Specific and Strain-Dependent Effects of Early Life Adversity on Behavioral and Epigenetic Outcomes

Long-term effects of early-life caregiving experiences onbrain-derived neurotrophic factorhistone acetylation in the adult rat mPFC

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